Abstract
Genome reduction has been observed in many bacterial lineages that have adapted to specialized environments. The extreme genome degradation seen for obligate pathogens and symbionts appears to be dominated by genetic drift. In contrast, for free-living organisms with reduced genomes, the dominant force is proposed to be direct selection for smaller, streamlined genomes. Most variation in gene content for these free-living species is of “accessory” genes, which are commonly gained as large chromosomal islands that are adaptive for specialized traits such as pathogenicity. It is generally unclear, however, whether the process of accessory gene loss is largely driven by drift or selection. Here we demonstrate that selection for gene loss, and not a shortened genome, per se, drove massive, rapid reduction of accessory genes. In just 1,500 generations of experimental evolution, 80% of populations of Methylobacterium extorquens AM1 experienced nearly parallel deletions removing up to 10% of the genome from a megaplasmid present in this strain. The absence of these deletion events in a mutation accumulation experiment suggested that selection, rather than drift, has dominated the process. Reconstructing these deletions confirmed that they were beneficial in their selective regimes, but led to decreased performance in alternative environments. These results indicate that selection can be crucial in eliminating unnecessary genes during the early stages of adaptation to a specialized environment.
Highlights
Bacterial genomes have the potential to rapidly change their size and content as a result of various mechanisms such as deletion, duplication and horizontal gene transfer
Over 91% of the deletion events were due to homologous recombination between matching sequence regions, and of these, 86% were between co-directional pairs of one of the 142 insertion sequences (ISs) present in the genome of M. extorquens AM1 [23]
These data have provided a rare opportunity to demonstrate that selection for gene loss contributed to the repeated, large-scale removal of accessory functions from adapting genomes
Summary
Bacterial genomes have the potential to rapidly change their size and content as a result of various mechanisms such as deletion, duplication and horizontal gene transfer. Of primary importance is the effective population size (Ne) of a species, as this influences the efficacy of selection versus drift Repeated bottlenecks, such as those experienced by intracellular endosymbionts (which participate in little, if any horizontal gene transfer), result in tremendous rates of sequence change and ineffective selection to maintain functions required for hostindependent lifestyle. Even when present on the main chromosome accessory genes are often found as discrete genomic islands disrupting an otherwise syntenic chromosome between strains in a species This can result in gains or losses via various mechanisms such as homologous or site-specific recombination and phage integration/excision [12], resulting in punctuated large-scale gene content changes. Either drift or selection could contribute to genome reduction observed in nature, we lack direct evidence to distinguish between the lack of purifying selection to maintain
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